Activity Patterns of Eurasian Lynx Are Modulated by Light Regime

Transcription

RESEARCH ARTICLE
Activity Patterns of Eurasian Lynx Are
Modulated by Light Regime and Individual
Traits over a Wide Latitudinal Range
Marco Heurich1,2*, Anton Hilger3, Helmut Küchenhoff3, Henrik Andrén4,
Luděk Bufka5, Miha Krofel6, Jenny Mattisson7, John Odden7, Jens Persson4,
Geir R. Rauset4, Krzysztof Schmidt8, John D. C. Linnell7
OPEN ACCESS
Citation: Heurich M, Hilger A, Küchenhoff H,
Andrén H, Bufka L, et al. (2014) Activity Patterns of
Eurasian Lynx Are Modulated by Light Regime and
Individual Traits over a Wide Latitudinal
Range. PLoS ONE 9(12): e114143. doi:10.1371/
journal.pone.0114143
1. Bavarian Forest National Park, Department of Conservation and Research, Grafenau, Germany, 2. Chair of
Wildlife Ecology and Management, Albert Ludwig University of Freiburg, Freiburg, Germany, 3. Ludwig
Maximilian University Munich, Statistical Consulting Unit, Department of Statistics, Munich, Germany, 4.
Grimsö Wildlife Research Station, Department of Ecology, Swedish University of Agricultural Sciences,
Riddarhyttan, Sweden, 5. Department of Research and Nature Protection, Šumava National Park
Administration, Kašperské Hory, Czech Republic, 6. University of Ljubljana, Biotechnical Faculty, Ljubljana,
Slovenia, 7. Norwegian Institute for Nature Research, Trondheim, Norway, 8. Mammal Research Institute,
Polish Academy of Sciences, Białowieża, Poland
Editor: Shin Yamazaki, University of Texas
Southwestern Medical Center, United States of
America
*[email protected]
Received: August 11, 2014
Accepted: November 3, 2014
Published: December 17, 2014
Copyright: ß 2014 Heurich et al. This is an openaccess article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and reproduction in any medium, provided the original author
and source are credited.
Data Availability: The authors confirm that all data
underlying the findings are fully available without
restriction. All relevant data are within the paper
and its Supporting Information files.
Funding: Financial support was provided by the
EU program Interreg IV (Ziel 3), the Bavarian
Forest National Park Administration, the Swedish
Environmental Protection Agency, the Norwegian
Environmental agency, the Research Council of
Norway, the Nature Protection Divisions of the
County Governor’s Offices in Finnmark, Troms,
Buskerud, Oppland, Telemark and Vestfold
(Norway), the Reindeer Development Fund in
Norway, the Carnivore Management Boards in
regions 2, 3 and 8 (Norway), the World Wide Fund
for Nature (Sweden), the Swedish Research
Council for Environment, Agricultural Sciences and
Spatial Planning (Formas) and the private foundation Marie-Claire Cronstedts Stiftelse. The
funders had no role in study design, data collection
and analysis, decision to publish, or preparation of
the manuscript.
Competing Interests: The authors have declared
that no competing interests exist.
Abstract
The activity patterns of most terrestrial animals are regarded as being primarily
influenced by light, although other factors, such as sexual cycle and climatic
conditions, can modify the underlying patterns. However, most activity studies have
been limited to a single study area, which in turn limit the variability of light
conditions and other factors. Here we considered a range of variables that might
potentially influence the activity of a large carnivore, the Eurasian lynx, in a network
of studies conducted with identical methodology in different areas spanning
latitudes from 49˚79N in central Europe to 70˚009N in northern Scandinavia. The
variables considered both light conditions, ranging from a day with a complete day–
night cycle to polar night and polar day, as well as individual traits of the animals.
We analysed activity data of 38 individual free-ranging lynx equipped with GPScollars with acceleration sensors, covering more than 11,000 lynx days. Mixed
linear additive models revealed that the lynx activity level was not influenced by the
daily daylight duration and the activity pattern was bimodal, even during polar night
and polar day. The duration of the active phase of the activity cycle varied with the
widening and narrowing of the photoperiod. Activity varied significantly with
moonlight. Among adults, males were more active than females, and subadult lynx
were more active than adults. In polar regions, the amplitude of the lynx daily
activity pattern was low, likely as a result of the polycyclic activity pattern of their
main prey, reindeer. At lower latitudes, the basic lynx activity pattern peaked during
PLOS ONE | DOI:10.1371/journal.pone.0114143 December 17, 2014
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Lynx Activity
twilight, corresponding to the crepuscular activity pattern of the main prey, roe deer.
Our results indicated that the basic activity of lynx is independent of light conditions,
but is modified by both individual traits and the activity pattern of the locally most
important prey.
Introduction
The sequence of day and night is the dominant ‘‘Zeitgeber’’, which synchronizes
the internal clocks of most terrestrial organisms [1]. This functionality enables the
organisms to proactively adapt their biochemical and physiological processes and
their behaviour to the 24-h environment [2]. This general circadian pattern of
behaviour can be modified by changing environmental conditions, such as season
[3] and weather [4], or by social [5] and individual traits [6]. Also the avoidance
of predators [7] and humans [8, 9] or patterns of food availability [10] can
influence the activity of animals.
The circadian rhythm of felids is generally considered to be crepuscular or
nocturnal [11], although the anatomical structure of their eyes makes them well
suited to function under a wide range of light conditions [12]. The daily predatory
activity of felids with large geographic ranges varies from fully nocturnal to
circadian and seems to be flexible both among and within species [13]. Important
factors driving felid activity rhythms seem to be the activity of their main prey
[14–16], and nocturnal activity is a primitive form of antipredator behaviour that
has developed in eutherian mammals during the Mesozoic Era (Nocturnal
Bottleneck Hypothesis) to which predators have to respond [17]. For instance, the
activity of jaguars (Panthera onca) and pumas (Puma concolor) coincides with the
nocturnal activity of armadillos (Dasypus novemcintus) and pacas (Aguti paca)
[18]. Similarly, pumas and Andean cats (Leopardus jacobita) in the High Andes
follow the activity of mountain vizcachas (Lagidium viscacia) [7]. Also lions
(Panthera leo) take advantage of prey vulnerability, stalking at night in plains with
little cover and diurnally in forests when prey congregates along rivers [19].
Previous studies of Eurasian lynx have shown that the species has a nocturnal or
crepuscular rhythm of activity, which has been shown to vary markedly with
temperature, sex, reproductive status and prey behaviour [14, 15, 20, 21]. The
activity of reproducing females is less nocturnal than that of adult males, although
the duration of total daily activity of both sexes is similar [14]. The general pattern
of activity of both males and females does not change over the year, but males are
active longer during the mating season as they also travel longer distances and
cover larger ranges, and females travel less when they have small kittens
[14, 15, 22, 23].
Most studies of carnivore activity patterns, including studies of lynx, have been
conducted within single study sites or geographically limited regions with a
relatively constant day–night cycle. But at high or low latitudes, where the sun
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Lynx Activity
remains constantly above the horizon (polar day) or below the horizon (polar
night) during the peak of summer and winter, a constant periodicity seems to be
of no advantage [24]. van Oort et al. [25] found that reindeer (Rangifer tarandus)
on the high arctic islands of Svalbard, with associated polar nights and polar days,
do not exhibit the 24-h locomotor periodicity observed in central Norway, which
has a day–night cycle. Instead, reindeer activity is polycyclic and determined by
the rumination cycle. The authors conclude that species have no selective
advantage in maintaining daily cycles in a non-rhythmic environment. They
further hypothesized that in the absence of a circadian rhythmicity, the activity of
herbivorous animals is controlled by their feeding cycles, and as a consequence,
also the activity patterns of predators preying on reindeer should adapt during
polar night and polar day.
The light intensity between new moon and full moon ranges over three orders
of magnitude [26]. Moonlight therefore may influence the activity of nocturnal
carnivores that detect their prey visually, i.e. when light intensity increases, the
predator should be able to detect and catch prey more easily. On the other hand,
moonlight might reduce predation risk if the predators need darkness to
successfully attack visually-oriented prey [27]. Only a few empirical studies have
assessed the role of the moon phase on the activity of felid predators and their
prey [18, 27, 28]. These studies indicate that the response of prey species to
moonlight also influences the activity of the predator. For example, moon phase
has no overall positive influence on jaguar activity levels, but when armadillos,
their most important prey, avoided foraging above ground during moonlight
nights, jaguar activity declined [18]. The activity of bobcats (Lynx rufus) was lower
on nights with a new moon and higher during full moon; this pattern was related
to the activity of their prey species, mostly small mammals, which move and
forage less during high lunar illumination to reduce predation risk [28]. Because
no study has indicated an influence of moonlight on the activity of the lynx prey
species red deer, roe deer and reindeer and because lynx is an efficient stalking
predator that can use any hiding cover to approach its prey, lynx are believed to
hunt successfully with or without illumination by moonlight.
In this study, we analysed the activity patterns of Eurasian lynx along a .20
degree latitudinal range with major differences in light conditions, ranging from
areas in the south that always have a complete day–night cycle to areas in the
north with polar night and polar day. Our objective was to use this immense
degree of variation in light cycle to disentangle the relative impacts of different
external and internal factors on lynx activity. Based on what is known about
carnivore activity patterns, we tested the following predictions: (1) the general
activity level is not influenced by daylight duration, (2) the animals exhibit a
crepuscular behaviour during the time of year with a full day–night cycle, (3) the
animals show distinct circadian patterns also during polar day and polar night, (4)
lynx activity remains constant with increasing intensity of moonlight, and (5) lynx
activity will vary with individual traits, such as sex and age, as reported in previous
studies of one locality, regardless of light conditions at different latitudes.
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Lynx Activity
Materials and Methods
Data collection and study sites
We analysed activity patterns of 38 individual Eurasian lynx, using data from four
study sites distributed over a latitudinal range of 20 degrees from central Europe
to northern Scandinavia (Fig. 1). Detailed information about the study sites can
be found in S1 Table and S2 Table.
Lynx were captured following established protocols using a range of methods,
including foot snares placed at fresh kills, box traps, darting from a helicopter, and
chasing lynx into trees with dogs (Sweden and Norway: [29, 30]; Bavaria,
Germany/Czech Republic: [31]). The captured lynx were equipped with GPS
collars with either GSM or VHF/UHF download (GPS plus mini, Vectronic
Aerospace GmbH, Berlin, Germany). Individuals in Sarek, northern Sweden, were
additionally equipped with intraperitoneally implanted VHF transmitters (IMP/
400/L, Telonics Inc., Mesa, AZ, USA) for long-term monitoring. When possible,
lynx were recaptured to replace the collar when the battery was depleted. The
handling protocol has been approved by the Swedish Animal Ethics Committee,
the Norwegian Experimental Animal Ethics Committee, and the Ethics
Committee of the Government of Upper Bavaria and fulfils their ethical
requirements for research on wild animals. In addition, permits for wild animal
capture were obtained from the Swedish Environmental Protection Agency, the
Norwegian Environmental Agency, and the Government of Lower Bavaria.
The collars also carried an analogue dual-axis accelerometer, which has a
dynamic range from 22G to +2G. One axis (axis x) measures acceleration in
forward/backward motion, and the other axis (axis y) measures sideward and
rotary motion. Changes in static acceleration (gravity) and dynamic acceleration
(collar) were measured every 8th second and averaged for 5-min intervals. The
value scale ranged from 0 (no activity) to 255 (22G/+2G). Since the x- and yactivity data are highly correlated [32, 33], we only analysed the x-activity data.
We monitored the lynx during periods of different length (min. 62 days, max. 777
days, mean 289 days). We acquired a total of 3,291,947 data points of activity at 5min intervals for a total of 11,186 monitoring days (Table 1). We only used collars
with the same type of activity sensors and firmware, as specified by the
manufacturer.
The activity sensors in the collars were sensitive enough to register all
movement including head shaking. Based on a previous validation study, we
determined that acceleration sensor values from 0 to 27 indicated inactive
behaviour [15]. Therefore, we considered the values above 27 as ‘‘active’’, which
likely includes all types of activity (e.g. walking, running, hunting, and
interacting). For the analyses, the portion of time (0–100%) the lynx spent active
(values.27) in 60-min intervals (activity per hour) was aggregated, as was activity
during different time phases of the day, e.g. twilight and night (activity per day
phase). In the following, the term activity refers to the percentage of time the lynx
were active (values .27).
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Fig. 1. Map of Western Europe with the locations of the four study sites. (See S1 Table ‘‘General
characteristics of the study sites’’, for a detailed description).
doi:10.1371/journal.pone.0114143.g001
We obtained times of sunrise/sunset and nautical twilight (centre of the sun is
geometrically 12 degrees below the horizon) from the US Naval Observatory using
the Naval Oceanography Portal (http://www.usno.navy.mil).
The data which forms the basis for the analysis can be found in S1 Dataset.
Data analysis
To visualize the activity patterns, we first displayed the acceleration data as an
actogram for each study site separately. Actograms illustrate the fine-scale activity
pattern of individuals in more detail than plots showing aggregated values for all
animals, and are a good demonstration of either variability or constancy of
pattern [34]. Then we plotted monthly 24-h patterns of activity for the different
seasons and study sites, averaging the portion of time active according to study
site and months of the year. All activity data is presented as the portion of time
Table 1. Distribution of studied lynx according to study site and status and description of the available data.
Area
Number
of lynx
Sex
(m/f)
Age (years)
(subadult/adult)
Observations
(5 min)
Observations
(60 min)
Observations
(days)
Bavaria-Czech Republic
8
5/3
1/7
666,985
54,840
2,272
Southern Norway
7
4/3
3/4
568,848
47,064
1,950
Northern Sweden
11
3/8
1/10
1,059,765
86,904
3,615
Northern Norway
12
6/6
2/10
996,349
80,568
3,349
Sum
38
18/20
7/31
3,291,947
269,376
11,186
doi:10.1371/journal.pone.0114143.t001
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Lynx Activity
active (0–100%). For example, an activity of 0.4 means that the lynx was active
40% of the time (i.e. with acceleration sensor values .27).
We estimated a linear mixed additive model [35, 36] with the response variable
percentage of time the lynx spent active per hour:
ACTit ~b0 zb1 x1it z:::zbp xpit zf (time of the day)zti z"it
ACTit denotes the activity of animal i at time t, while xkit denotes the values of
explanatory variables listed in Table 2. The term f (time of the day) denotes a
flexible smooth function of the time of the day, while ti denotes a random
intercept for animal I, and eit is the error term. ti was included since we had
repeated measurements of the 38 individuals. The autocorrelation of the residuals
from the linear mixed model was 0.294 (lag 1) and 0.104 (lag 2). This is an
indication that the chosen models without auto-covariance terms are acceptable.
We used the p-splines to estimate the additive component. To verify the results of
the models, a sensitivity analysis was performed with a gamma generalized linear
mixed model. The results of these fittings were comparable; therefore, the linear
mixed model was deemed sufficient.
To check whether the activity patterns were dependent on general light
conditions, we fitted our model of activity to a data subset that compiled
observations during polar night (day on which the sun is below the horizon for
24 h), polar day (day on which the sun is above the horizon for 24 h) and equinox
(daylight duration between 11:00 and 13:00).
In the second analysis, we fitted models with the daily activity in different day
phases. We used the following outcome variables: activity per day (24 h), activity
during daylight, activity during twilight morning, activity during twilight evening
and activity during the night. The covariates in Table 2, but not the day phase and
daylight duration as a quadratic term, were included in these linear mixed models.
Note that these models include daily data.
The statistical significance level was set to 5%. The significance levels (p-values)
were estimated with a likelihood ratio test for the categorical covariables (e.g.
gender, season, age and region) and with a Wald test for all other non-categorical
covariables. For the statistical computing, we used the software R (version 2.14.0)
[37] and the library ‘‘nlme’’ and ‘‘mgcv’’.
Results
Descriptive analysis
The daily lynx activity showed a clear pattern, with the lowest activity during
midday and high activity during twilight and night, irrespective of the duration of
the day (Figs. 2 and 3). During spring and fall when days and nights were equally
long, the activity patterns in all study areas were similar, with a period of low
activity during the day and activity peaks during twilight evenings and twilight
mornings. Activity at night was lower than at twilight but higher than during the
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Table 2. Explanatory variables considered in the modelling approach.
Variable
Scale
Value range
Description
Individual
animal
Categorical
(1;38)
Lynx individual id
Daylight
duration
Continuous
(0;24)
Length of the day from sunset to sunrise
Moon phase
Continuous
(0;15)
05 new moon, 155full moon
Age
Categorical
Subadult; adult
Adult .1.5 years
Status
Categorical
Male, female,
female with kittens
Sex of the lynx and kittens confirmed
Season
Categorical
Spring, summer,
autumn, winter
Time of the year according to astronomical definition (21.3; 21.6; 23.9; 21.12)
Study site
Categorical
Bavaria-Czech Republic,
southern Norway, northern
Sweden, northern Norway
Study site
day. In September, activity was similar during twilight evenings and twilight
mornings; in March, activity was higher during twilight evenings, except for
southern Norway, where activity did not differ. In the Bavaria–Czech Republic
study area in June, activity peaked around sunrise and sunset. In southern Norway
during midsummer, the twilight activity peaks were not pronounced (i.e. not very
different from night-time levels), and the period of low activity during the day was
longer. During polar day in northern Sweden and northern Norway, activity did
not peak, but activity around noon was still lower than at midnight. In December
in Bavaria–Czech Republic and southern Norway, a pronounced activity peak was
observed only in the evening, but not in the morning. In northern Sweden and
northern Norway during polar nights, lynx activity was still lowest around noon,
but this period of low activity was short; during the rest of the day, activity was
higher but without peaks after or before noon. Figs. 2 and 3 also show that the
duration of the active phase of the activity cycle varied with the widening and
narrowing of the photoperiod.
Modelling approach
The model showed that the Eurasian lynx has a circadian activity pattern with low
activity around noon and high activity at twilight and night. The highest activity
was observed during twilight evenings, followed by twilight mornings and night
(Table 3). We observed that activity varied significantly with moon phase, but this
variation was very small. We did not find a significant interaction between moon
phase and study area.
Also the status of the animal significantly influenced its activity. Male lynx were
the most active, followed by females with kittens and then females without kittens.
Generally, subadult lynx were significantly more active than adults. Also activity
varied significantly with season (with autumn as the reference category) (Table 3).
Lynx were more active in autumn and summer than in spring and winter. Lynx
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Fig. 2. Actograms of Eurasian lynx activity at the four study sites. Activity was measured as forwards-backwards acceleration on a relative scale from 0
to 255. The x-axes indicate the hours of the day (from 0 to 24 UTC; coordinated universal time). The y-axes indicate the days of the year, with each
horizontal line representing one day, from January 1 (top line) to December 31 (bottom line). Each coloured pixel corresponds to one mean activity value at
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one time interval of 5 min averaged over the number of lynx in the corresponding region, ranging from dark blue for little or no activity to red for high activity.
Curved black lines from left to right indicate beginning of nautical twilight, sunrise, sunset, and end of nautical twilight.
activity decreased from northern to southern latitudes (highest in northern
Norway, lowest in Bavaria-Czech Republic).
We included the time of day with an additive term (p-spline) in the model of
the activity per hour and adjusted for the other covariates (Fig. 4). Activity was
lowest at 12:00 (noon) and thereafter increased steadily to the highest level at
20:00 (twilight evening, early night). Activity remained high until early morning,
with values.0.4 (lynx active 40% of the time). After morning, the activity level
decreased to its minimum level at noon. The 95% confidence level for the
predicted activity of these values and the following estimations were narrow;
therefore, the 95% confidence intervals are not shown in the figures.
Season-specific models showed that even during polar night and polar day,
activity around noon was low. However, the period of low activity was shorter
Fig. 3. Eurasian lynx daily activity at the four study sites. Each plot shows the portion of time spent active per hour (activity) over the course of a day in
the month and averaged over the number of lynx in the area indicated. Dashed vertical lines, sunset and sunrise; dotted lines, beginning and end of twilight.
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Table 3. Results of the linear mixed additive model with the response variable set to the percentage of time active per hour.
Variable
Estimate
Intercept
0.3354
Day
0
Night
0.0204
Twilight evening
0.1404
Twilight morning
0.1151
Moon
20.0002
Females
0
Females with kittens
0.0209
Male
0.0337
Adult
0
Subadult
0.0349
Autumn
0
Spring
20.0345
Summer
20.0003
Winter
20.0332
Bavaria-Czech Republic
0
Southern Norway
0.0123
Northern Sweden
0.0242
Northern Norway
0.0308
R2 adj.
0.157
p-value
,0.001
0.005
,0.001
0.011
,0.001
0.129
during polar night and longer and less pronounced during polar day. Also during
polar day, activity did not peak before or after the noon low. During equinox,
activity peaked at twilight morning (4:00) and at twilight evening (20:00) (Fig. 4).
The differences in the predicted activity patterns around equinox, polar night and
Fig. 4. Lynx activity predicted by the linear mixed additive model for the response variable portion of
time spent active per hour during one day (activity) a) throughout the year, and b) subsets of data
representing different light conditions. Each covariable is predicted for the reference category adult,
female, autumn, Bavaria–Czech Republic, and full moon (50); therefore, only time influences the activity.
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polar day (Fig. 4) indicated an important influence of daylight duration on the
lynx daily activity pattern.
In our second analysis, we assessed the association between activity during the
four day phases (twilight morning, day, twilight evening, and night) and daylight
duration. The general 24-h activity level of the animals was not associated with the
daylight duration (Fig. 5). The allocation of activity to the different day phases
changed with respect to daylight duration (Fig. 5). The highest activity was during
twilight evening, followed by twilight morning, night and day. Only when the
daylight duration was very short did the night activity increase. With increasing
daylight duration, activity at twilight evening strongly increased and reached a
peak at 17 h of daylight and afterwards decreased again. Activity at twilight
morning and during the day increased almost linearly with increasing daylight,
whereas activity at night increased only slightly. The estimators for the other
covariates are in line with those of the main model and are given in S3 Table.
Model output of the linear mixed additive model for the response variable portion
of active time for the whole day (24 h) and the phases day, twilight morning,
twilight evening and night.
Discussion
Our analysis of lynx activity patterns over a wide latitudinal range revealed as
predicted that the overall daily activity level was not influenced by daylight
duration. The distinct circadian pattern was even kept during polar night and
polar day. However, the lynx activity pattern significantly varied with daylight
duration. First, activity during twilight evening and twilight morning peaked on
days with a full day–night cycle, as has been already shown in other studies
[14, 15], while the amplitude of circadian variation in activity was lower during
polar night and polar day. Second, the active phase (5 alpha) was longer in
summer than in winter. Contrary to our expectations, lynx activity varied
significantly with moon phase, but this variation was very small. As predicted,
subadult lynx were more active than adults. Among the adults, male lynx were
more active than females, and females with kittens were more active than solitary
females. Lynx were most active in autumn and summer. The general activity level
in the study sites decreased from north to south.
We identified bimodal lynx activity patterns with lowest activity at midday and
highest activity after sunset or before sunrise, although the variation of activity
was lower in the polar environment. This finding for lynx in regions with polar
nights and polar days contradicts the suggestions of van Oort et al. [25] for species
living in polar environments. The polycyclic activity pattern of reindeer observed
by these authors is probably reindeer specific and cannot be generalized for other
species, or at least not for carnivores. This interpretation is in accordance with
molecular evidence, which has shown that reindeer lack mechanisms for
generating circadian rhythmicity [38], which seems to be a specific adaptation of
this species. In contrast to reindeer, Eurasian lynx distribution is not limited to
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Fig. 5. Lynx activity predicted by the linear mixed additive model for the response variable portion of
time spent active (activity) for one 24–h period (whole day) and during the phases day, twilight
morning, twilight evening and night depending on daylight duration. Each covariable is predicted for the
reference category adult, female, autumn, Bavaria–Czech Republic, full moon (50); therefore, only daylight
influences the activity.
polar and boreal environments and covers a wide latitudinal range from northern
Russia to northern India and the Mediterranean. Therefore, lynx physiology is
adapted to a 24-h rhythm ruled by the day–night cycle. However, the general
circadian pattern of lynx was adapted to the different light regimes. This could be
seen in the smaller amplitude of activity during polar day and polar night than at
equinox and a shorter period of the amplitude during polar day than polar night
as well as lack of activity peaks at high latitudes during polar day and polar night.
Our results of lynx activity at lower latitudes and at times around the equinox
support results of previous studies from Central Europe in areas with a complete
day–night cycle [14, 15, 20]. In these areas, lynx activity is lowest during the day
and highest at night, with peaks at twilight. This can be interpreted as the animals
spending their days at a lair and hunting and feeding in the evening and night.
Such a crepuscular activity pattern has also been shown for other felids, such as
Canadian lynx (Lynx canadensis) [39], bobcat [40], Iberian lynx [41] and tiger
(Panthera tigris) [42]. This pattern is probably strongly influenced by the activity
patterns of their primary prey and the lynx hunting technique. Several studies
have shown that red deer and roe deer, the principal prey of Eurasian lynx in the
southern study regions, also have a clear crepuscular activity pattern [34, 43–46].
Lynx activity followed these crepuscular activity peaks, but was also high during
the night, when deer are less active. One reason for this could be that darkness
gives increased cover to the lynx, thereby impeding visual detection by the prey,
which is crucial for a stalking predator. Their prey species rely more on olfactory
or auditory information at night, whereas lynx, with their superior visual senses
[11], might be more successful in catching prey during the night. Our results
indicated that lynx activity patterns seem to follow that of its prey species. The
lynx show pronounced bimodal activity peaks when the main prey species (red
deer and roe deer) show bimodal activity during twilight and less pronounced
activity peaks when the main prey species (reindeer) have a polycyclic activity
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Lynx Activity
pattern with no distinct peaks in activity at twilight [47]. Another reason for the
crepuscular and night activity could be the avoidance of human activity, which
has been shown to strongly influence circadian behaviour patterns of several
carnivores [48–51]. This argumentation is supported by the fact that in all study
regions, human persecution (either legal or illegal) is the main cause of lynx death,
which might lead to the lynx behavioural adaption of avoiding periods when
people are most active [52, 53]. On the other hand, lynx persecution by humans is
a very young phenomenon from an evolutionary perspective, yet nocturnal
activity of mammals is hypothesized to date back millions of years [17]. Therefore,
human persecution might simply reinforce an innate characteristic and might not
be the ultimate cause of the observed activity pattern. This interpretation is also
supported by the finding that lynx activity was highest during twilight evening
when human activity was also highest. If human disturbance was a major driver of
lynx activity, one would in contrast expect highest lynx activity during twilight
morning when human activity is lower.
The general 24-h activity level of the lynx was constant despite changes in
daylight duration. This result shows that lynx do not have to be active longer, for
example, to obtain enough food as the daylight duration increases. Consequently,
it does not appear that hunting success is dependent on the day–night cycle
because a lower hunting success would need to be compensated for by a higher
hunting effort, which would lead to a higher activity level [54]. However, the
timing of activity allocation changed with increasing daylight duration. The
daytime activity level was lower than the activity level during all other day phases
but increased with daylight duration. Despite this, night-time activity only slightly
increased. Highest activity was at twilight evening, followed by twilight morning.
Given the frequency of this pattern among carnivores, it seems that crepuscular
and nocturnal activities are driven by optimal hunting conditions [55].
Theuerkauf et al. [10] argue that wolves can most easily detect prey under dim
light conditions that occur on moonlight nights or at twilight. Although we
identified lynx activity peaks at twilight, the moon phase did not have a
meaningful influence on lynx activity, even though light conditions during nights
with bright moon phases are similar to those at twilight. Therefore, light
condition is probably not as important a factor as prey activity, as has been shown
for some other carnivores, e.g. lions [56]. However, moonlight does not seem to
influence the nocturnal activity levels of roe deer [45]. Accordingly, lynx have no
advantage in increasing their activity at full moon, but would have an advantage at
twilight, when roe deer are most active. Also puma activity does not vary with the
level of moonlight, and jaguar activity even declines with increased moonlight
[18]. On the other hand, African lions are less successful in obtaining prey on
moonlit nights [27]. The effect of moonlight might also be masked by the weather.
Clouds during full moon might result in the same light conditions as with no
moon. We were not able to include local weather parameters in our study, but
because of the large sample size, it should have been possible to detect a significant
overall influence even without considering detailed weather parameters.
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Lynx Activity
By studying lynx activity over a large geographic range, we tested whether lynx
activity patterns already known for lynx in central Europe are characteristic across
a wider part of their distribution. As previously shown, demographic differences
in activity levels may be due to the energetic/physiological demands associated
with social and reproductive behaviours. The home ranges of males of this
polygamous species encompass the home ranges of several females [57, 58]. To
patrol these large home ranges, males must cover larger distances than females,
and this is reflected in the higher activity of males. Such a pattern has also been
documented for male mountain lions [59]. In contrast to our results, Schmidt
[14] found that the activities of female and male lynx were similar. They argued
that although males have to allocate more time to patrolling their larger home
range, females with kittens have to kill on average 1.5 times more deer per time
unit [60]. We were also able to confirm that female lynx with kittens had a higher
mean activity than females without kittens. At first glance, this result does not
seem to follow expectations, as females with kittens stay longer in the den to
lactate and warm the offspring. However, the denning period is actually short (6–
8 weeks) and falls within the warmest period of the year (parturition end of May/
beginning of June), and the females must intensively hunt afterwards because of
their high energy needs during lactation. In addition, kittens are not able to follow
their mother from kill to kill until late summer or autumn. Before this time,
females have to return to the den after every hunt and for each feeding bout,
which results in a much higher distance travelled. In addition, females with kittens
have to hunt and kill more prey than females without kittens, which results in
more activity [14, 22, 60–63]. In contrast, in northern Norway, females with
kittens and females without kittens have the same kill rates, probably because of
high densities of available prey [61]. The activity of female lynx with kittens
increased during the day and in the morning; such a pattern has also been
observed in previous studies of Eurasian lynx [14] [20] and for Canadian lynx
[39].
Sub-adult lynx, which disperse between January to April [64], were more active
across the 24-h period and during the day than adult individuals. The same
behaviour was observed for Iberian lynx in their first year, although the diurnal
activity decreased thereafter [4], and for African lions [65], and is believed to be a
general pattern of nocturnal species [66]. Sub-adult animals have to leave their
natal home range and search for areas not occupied by adult animals. In that time,
they have to disperse over large distances, which might influence activity [64, 67].
Probably even more important is that the sub-adults are not experienced hunters
and do not know where to find prey in unfamiliar areas. Therefore, it can be
expected that they have to cover large distances and have a higher hunting effort,
which increases overall activity levels. Higher activity during the day could be
advantageous because the sub-adults might thereby minimize interactions with
dominant territory holders, who are more active during twilight and at night [65]
and who would aggressively drive the sub-adults out of their home range [68, 69].
Lynx were in general more active in autumn and summer than in spring and
winter. We hypothesized that they would be more active in winter and during the
14 / 20
Lynx Activity
mating season (February/March), when males move over longer distances to
secure females for mating and when territorial marking is most intensive [70].
Also the kittens are larger in winter, requiring more prey to be supplied by the
females. However, it is easier to hunt in winter because snow cover limits the
mobility of their prey, while the movement of lynx is less affected [34, 45].
Moreover prey species are often clustered around feeding stations or on open
ridges where snow is blown away [71]. At such sites, lynx can find prey without a
high searching effort. Also meat decomposition is slower in winter, and it has been
shown that the role of scavenging is not as important in that season [72]. During
summer and autumn, prey is more dispersed, and the hunting effort is therefore
probably higher. Also predation may include more neonates in summer and a
higher loss of meat by invertebrate and vertebrate scavengers [72, 73], which
would result in higher predation rates and a higher overall activity level. In
addition, the observed seasonal differences can also depend on weather features,
such as snow cover, which can hinder movements over large distances.
Lynx activity increased with latitude and was higher in northern study sites than
in southern study sites. This difference could be related to a multitude of factors
because the study site is a surrogate of different factors, such as various
environmental conditions, different levels of human impact and different prey
species. But it is likely that the observed differences are related to the size of the
home ranges, which are 6 (males) to 8 (females) times larger in northern Norway
(S2 Table Lynx density, hunting, prey species and light conditions of the study
sites), and to the subsequent lower densities [74]. Therefore, the lynx have to
travel longer distances to patrol their territory and to search for prey, forcing them
to be more active [54].
The Eurasian lynx, with its large geographical distribution across Eurasia, shows
a general circadian activity pattern with low activity at noon and high activity at
night. Even during polar night and polar day, this general pattern is kept;
however, it was modulated such that the differences between night-time and
daytime activity were not as pronounced during polar night and the period with
low activity was shorter during polar night.
Our results showed that the general activity level of the Eurasian lynx is the
same regardless of light conditions and that only relative activity levels during
different parts of the day and the distinctness of activity peaks change, being more
or less pronounced. Therefore, we conclude that the lynx circadian, bimodal
activity pattern is stable throughout the lynx range, even when polycyclic prey are
hunted. According to historical records, the colonization of the northernmost
range in Scandinavia was very recent, starting in the 1960s and reaching Finnmark
(the northernmost study site) in the early 1990s [75]. Perhaps the observed
activity patterns in the far north are only a relict characteristic with a genetic basis
from lower latitudes, where activity was highly adaptive. These patterns might
have been conserved in the subarctic biomes because of the short time interval and
because maintaining these patterns incurs no cost. For the Eurasian lynx, light
conditions do not appear to be the limiting factor for their hunting strategy as a
stalking predator as they do not have to compensate for lack of darkness as cover
15 / 20
Lynx Activity
and do not have to adapt to variable light conditions owing to moon phases.
These points indicate that a crepuscular activity schedule provides an optimal
hunting strategy, which enables a mid-sized carnivore to have a generalized diet
and wide distribution.
In future research, other factors influencing Eurasian lynx activity have to be
taken into consideration. First, the interaction of Eurasian lynx behaviour with
fine temporal scale environmental conditions, such as temperature and snow,
would provide information on how weather parameters influence the animals in
different regions. This would form the basis for understanding how global change
might influence the observed patterns. Second, as prey activity is an important
driving factor of predator activity, simultaneous studies of predator and prey
activities would be informative. Third, to evaluate anthropogenic factors,
comparison of activity patterns of populations exposed to various levels of
exploitation could reveal whether crepuscular and nocturnal activity patterns
either are influenced by the environmental or have a genetic basis. Finally, we
hope that this study will inspire other comparative analyses of activity data of
other species, especially common prey species with similarly wide latitudinal
distributions. The widespread use of GPS collars with activity sensors should allow
the generation of vast amounts of untapped data that could be used to explore the
relative impacts of a diversity of internal and external factors on animal
chronobiology.
Supporting Information
S1 Table. General characteristics of the study sites.
doi:10.1371/journal.pone.0114143.s001 (DOCX)
S2 Table. Lynx density, hunting, prey species and light conditions of the study
sites.
S3 Table. Model output of the linear mixed additive model for the response
variable portion of active time for the whole day (24 h) and the phases day,
twilight morning, twilight evening and night.
S1 Dataset. Data table, R-Code.
doi:10.1371/journal.pone.0114143.s004 (ZIP)
Acknowledgments
This study is part of the Scandinavian lynx research programme, Scandlynx, and a
project on the predator–prey relationship of Eurasian lynx, red deer and roe deer
carried out by the Bavarian Forest National Park Administration, Department of
Research and Documentation, and a long-term research project on the Eurasian
lynx in the Šumava National Park. We thank Karen A. Brune for language revision
16 / 20
Lynx Activity
and Peter Segerström, Einar Segerström, Thomas Strømseth, Jon M. Arnemo,
Horst Burghart, Martin Gahbauer, Martin Horn and Oldřich Vojtěch and many
others for their cooperation during field work, and Julia Schiele for the statistical
analysis during her statistical consulting work. Last but not least we thank Nina
Kelch for map production.
Author Contributions
Conceived and designed the experiments: MH LB HA JL JO. Performed the
experiments: MH HA LB JM JP GR JL JO. Analyzed the data: AH HK MH.
Contributed to the writing of the manuscript: MH AH HK HA MK JM JP GR KS
JL JO.
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Activity Patterns of Eurasian Lynx Are Modulated by Light Regime

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